Management of Biological Invasions (2019) Volume 10, Issue 4: 602–616 Special Issue: Marine Invasive Species Guest editors: Stephan Bullard, Mary Carman and Joana Dias CORRECTED PROOF Research Article Biogeographical patterns of tunicates utilizing eelgrass as substrate in the western North Atlantic between 39o and 47o north latitude (New Jersey to Newfoundland) Mary R. Carman1,*, Philip D. Colarusso2, Hilary A. Neckles3, Paul Bologna4, Scott Caines5, John D.P. Davidson6, N. Tay Evans7, Sophia E. Fox8, David W. Grunden9, Sarah Hoffman4, Kevin C.K. Ma10, Kyle Matheson5, Cynthia H. McKenzie5, Eric P. Nelson2, Holly Plaisted11, Emily Reddington12, Stephen Schott13 and Melisa C. Wong14 1Woods Hole Oceanographic Institution, Woods Hole, Massachusetts 02543, USA; 2US Environmental Protection Agency, Boston, Massachusetts 02109, USA; 3U.S. Geological Survey Patuxent Wildlife Research Center, Augusta, Maine 04330, USA; 4Montclair State University, Montclair, New Jersey 07043, USA; 5Fisheries and Oceans Canada, St. John’s, Newfoundland and Labrador A1C 5X1, Canada; 6Fisheries and Oceans Canada, Charlottetown, Prince Edward Island C1E 2A1, Canada; 7Massachusetts Division of Marine Fisheries, Gloucester, Massachusetts 01930, USA; 8US National Park Service, Cape Cod National Seashore, Eastham, Massachusetts 02667, USA; 9Oak Bluffs Shellfish Department, Oak Bluffs, Massachusetts 02557, USA; 10Laval University, Quebec City, Quebec G1V 0A6, Canada; 11US National Park Service, Northeast Coastal and Barrier Network, Narragansett, Rhode Island 02881, USA; 12Great Pond Foundation, Edgartown, Massachusetts 02539, USA; 13Cornell University Cooperative Extension, Southold, New York 11971, USA; 14Fisheries and Oceans Canada, Dartmouth, Nova Scotia B2Y 4A2, Canada E-mail: [email protected] (MC), [email protected] (PC), [email protected] (HN), [email protected] (PB), [email protected] (SC), [email protected] (JD), [email protected] (NE), [email protected] (SF), [email protected] (DG), [email protected] (SH), [email protected] (KM), [email protected] (KM), [email protected] (CM), [email protected] (EN), [email protected] (HP), [email protected] (ER), [email protected] (SS), [email protected] (MW) *Corresponding author Co-Editors’ Note: This study was first presented at the 2018 International Invasive Abstract Sea Squirt Conference held at Woods Hole, Massachusetts, USA, May 2-4, 2018 (https:// Colonization of eelgrass (Zostera marina L.) by tunicates can lead to reduced plant web.whoi.edu/sea-squirt-conference/). Since growth and survival. Several of the tunicate species that are found on eelgrass in its inception in 2005, the IISSC series has the northwest Atlantic are highly aggressive colonizers, and range expansions are provided a venue for marine biologists predicted in association with climate-change induced increases in seawater and people concerned with invasive ascidians, to explore the biology, ecology, temperature. In 2017, we surveyed tunicates within eelgrass meadows at 33 sites impacts, management options for control, from New Jersey to Newfoundland. Eight tunicate species were identified colonizing and other relevant topics. eelgrass, of which four were non-native and one was cryptogenic. The most Citation: Carman MR, Colarusso PD, common species (Botrylloides violaceus and Botryllus schlosseri) occurred from Neckles HA, Bologna P, Caines S, Davidson New York to Atlantic Canada. Tunicate faunas attached to eelgrass were less JDP, Evans NT, Fox SE, Grunden DW, diverse north of Cape Cod, Massachusetts. Artificial substrates in the vicinity of the Hoffman S, Ma KCK, Matheson K, eelgrass meadows generally supported more tunicate species than did the eelgrass, McKenzie CH, Nelson EP, Plaisted H, Reddington E, Schott S, Wong MC (2019) but fewer species co-occurred in northern sites than southern sites. The latitudinal Biogeographical patterns of tunicates utilizing gradient in tunicate diversity corresponded to gradients of summertime sea surface eelgrass as substrate in the western North temperature and traditional biogeographical zones in the northwest Atlantic, where Atlantic between 39o and 47o north latitude Cape Cod represents a transition between cold-water and warm-water invertebrate (New Jersey to Newfoundland). Management of Biological Invasions 10(4): faunas. Tunicate density in the eelgrass meadows was low, ranging generally from 602–616, https://doi.org/10.3391/mbi.2019.10.4.02 1–25% cover of eelgrass shoots, suggesting that space availability does not Received: 12 July 2019 currently limit tunicate colonization of eelgrass. This survey, along with our 2013 survey, provide a baseline for identifying future changes in tunicate distribution and Accepted: 9 September 2019 abundance in northwest Atlantic eelgrass meadows. Published: 30 October 2019 Handling editor: Stephan Bullard Copyright: © Carman et al. Key words: regional study, Zostera marina, fouling organisms, Ascidiacea, introduced This is an open access article distributed under terms species of the Creative Commons Attribution License (Attribution 4.0 International - CC BY 4.0). OPEN ACCESS. Carman et al. (2019), Management of Biological Invasions 10(4): 602–616, https://doi.org/10.3391/mbi.2019.10.4.02 602 Biogeographical patterns of tunicates Introduction The prevalence and distribution of non-native tunicates on a wide variety of substrates in the northwest Atlantic has been increasing (Bullard et al. 2007; Locke et al. 2007; Sargent et al. 2013; Moore et al. 2014; Carman et al. 2016). In addition, expansion to new substrates, such as the submerged vascular plant Zostera marina Linneaus, 1753 (eelgrass) has been documented for a number of tunicate species (Carman and Grunden 2010; Carman et al. 2014). Colonization of eelgrass by tunicates can cause reduced growth, production, and even mortality of eelgrass shoots (Wong and Vercaemer 2012; Long and Grosholz 2015). Eelgrass is considered a foundational species that serves many critical ecological functions. It is highly productive and is widely recognized for its importance in coastal food webs and as a nursery and refuge habitat for many fish and invertebrate species (Thayer et al. 1985; Heck et al. 1995; Lazzari et al. 2003). Eelgrass stabilizes sediments and provides some shoreline protection and erosion control (Thayer et al. 1985). In addition, by sequestering large quantities of carbon, eelgrass may buffer climate change (Fourqurean et al. 2012; Colarusso et al. 2016a). Distribution and abundance of eelgrass has declined substantially in the northwest Atlantic from direct physical disturbance by dredging, dock and pier construction, and damage from boats and moorings (Burdick and Short 1999; Orth et al. 2017) and indirect effects of watershed disturbance from development that leads to reduced water clarity (Hauxwell et al. 2003; Lee et al. 2007). Colonization of eelgrass by tunicates increases stress on eelgrass plants, which could hasten losses of this important habitat. In 2013, the first tunicate survey of northwest Atlantic eelgrass meadows was conducted to determine the extent of colonization in the region (Carman et al. 2016). In that survey, twenty-one sites between Newfoundland and New Jersey were surveyed, and a total of 8 species of tunicates were found colonizing eelgrass. Four of those 8 colonizers are considered non- native. The most common tunicates present were Botryllus schlosseri (Pallas, 1766) and Botrylloides violaceus Oka, 1927. In general, tunicate coverage of eelgrass shoots was < 25%, though it approached 75–100% in some locations, and several of the tunicate species found on eelgrass at that time (B. schlosseri, B. violaceus, Ciona intestinalis (Linneaus, 1767), and Didemnum vexillum Kott, 2002) are considered highly aggressive colonizers (Carver et al. 2006; Bullard et al. 2007; Epelbaum et al. 2009). Among marine fouling communities, seawater temperature governs species growth rates and competitive abilities (Lord 2016), and temperature increases are expected to strongly influence changes in community composition (Hansen et al. 2006; Lord and Whitlatch 2015). Water temperatures are expected to increase 2–4 °C in the northwest Atlantic by 2100 (IPCC 2007). The 2013 eelgrass tunicate survey showed fewer tunicate Carman et al. (2019), Management of Biological Invasions 10(4): 602–616, https://doi.org/10.3391/mbi.2019.10.4.02 603 Biogeographical patterns of tunicates Figure 1. Map of study sites and tunicate species occurrences on eelgrass. species in northern than in southern eelgrass meadows (Carman et al. 2016). Range expansions are predicted for non-native and native species in association with climate-induced changes in seawater temperature (Parmesan et al. 2005; Rius et al. 2014). Colder sites, often characterized by more open space available, are likely the most susceptible to future invasions. As climate change extends the ranges of potential invaders (Lord 2016), eelgrass may provide substrate for expansion of tunicate species. Thus, northern eelgrass meadows may see increases in the number of tunicate species and in tunicate overgrowth on eelgrass shoots. The purpose of this study was to improve understanding of the distribution, diversity, and abundance of tunicate species colonizing eelgrass along the northwest Atlantic coast. We revisited 11 sites that were surveyed in 2013, while adding more sites to the latitudinal gradient between New Jersey and Newfoundland. The result